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The human brain's complex morphology is spatially constrained by numerous intrinsic and extrinsic physical interactions. Spatial constraints help to identify the source of morphological variability and can be investigated by employing anatomical network analysis. Here, a model of human craniocerebral topology is presented, based on the bony elements of the skull at birth and a previously designed model of the brain. The goal was to investigate the topological components fundamental to the craniocerebral geometric balance, to identify underlying phenotypic patterns of spatial arrangement, and to understand how these patterns might have influenced the evolution of human brain morphology. Analysis of the craniocerebral network model revealed that the combined structure of the body and lesser wings of the sphenoid bone, the parahippocampal gyrus, and the parietal and ethmoid bones are susceptible to sustain and apply major spatial constraints that are likely to limit or channel their morphological evolution. The results also showcase a high level of global integration and efficient diffusion of biomechanical forces across the craniocerebral system, a fundamental aspect of morphological variability in terms of plasticity. Finally, community detection in the craniocerebral system highlights the concurrence of a longitudinal and a vertical modular partition. The former reflects the distinct morphogenetic environments of the three endocranial fossae, while the latter corresponds to those of the basicranium and calvaria.

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In adult humans, the orbits vary mostly in their orientation in relation to the frontal bone profile, while the orientation of the cranial base and face are associated with the anteroposterior dimensions of the parietal bone. Here we investigate the effect of parietal bone length on the orientation of the orbits, addressing craniofacial integration and head orientation. We applied shape analysis to a sample of computed tomography scans from 30 adult modern humans, capturing the outlines of the parietal and frontal bones, the orbits, and the lateral and midline cranial base, to investigate shape variation, covariation, and modularity. Results show that the orientation of the orbits varies in accordance with the anterior cranial base, and in association with changes in parietal bone longitudinal extension. Flatter, elongated parietal bones are associated with downwardly oriented orbits and cranial bases. Modularity analysis points to a significant integration among the orbits, anterior cranial base, and the frontal profile. While the orbits are morphologically integrated with the adjacent structures in terms of shape, the association with parietal bone size depends on the spatial relationship between the two blocks. Complementary changes in orbit and parietal bone might play a role in accommodating craniofacial variability and may contribute to maintain the functional axis of the head. To better understand how skull morphology and head posture relate, future studies should account for the spatial relationship between the head and the neck.

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Network analysis provides a quantitative tool to investigate the topological properties of a system. In anatomy, it can be employed to investigate the spatial organization of body parts according to their contiguity and patterns of physical contact. In this study, we build a model representing the spatial adjacency of the major regions of the human brain often considered in evolutionary neuroanatomy, to analyse its topological features. Results suggest that the frontal lobe is topologically independent of the posterior regions of the brain, which in turn are more integrated and influenced by reciprocal constraints. The precentral gyrus represents a hinge between the anterior and posterior blocks. The lateral temporal cortex is particularly influenced by the neighbouring regions, while the parietal cortex is minimally constrained by the overall brain organization. Beyond the reciprocal spatial influences among cortical areas, brain form is further constrained by spatial and mechanical influence of the braincase, including bone and connective elements. The anterior fossa and the parietal bones are the elements more sensitive to the brain-braincase spatial organization. These topological properties must be properly considered when making inferences on evolutionary variations and macroscopic differences of the human brain morphology.

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Evolutionary neuroanatomy must integrate two different sources of information, namely from fossil and from living species. Fossils supply information concerning the process of evolution, whereas living species supply information on the product of evolution. Unfortunately, the fossil record is partial and fragmented, and often cannot support validations for specific evolutionary hypotheses. Living species can provide more comprehensive indications, but they do not represent ancestral groups or primitive forms. Macaques or chimpanzees are frequently used as proxy for human ancestral conditions, despite the fact they are divergent and specialized lineages, with their own biological features. Similarly, in paleoanthropology independent lineages (such as Neanderthals) should not be confused with ancestral modern human stages. In this comparative framework, paleoneurology deals with the analysis of the endocranial cavity in extinct species, in order to make inferences on brain evolution. A main target of this field is to distinguish the endocranial variations due to brain changes, from those due to cranial constraints. Digital anatomy and computed morphometrics have provided major advances in this field. However, brains and endocasts can be hard to analyze with geometrical models, because of uncertainties due to the localization of cortical landmarks and boundaries. The study of the evolution of the parietal cortex supplies an interesting case-study in which paleontological and neontological data can integrate and test evolutionary hypotheses based on multiple sources of evidence. The relationships with visuospatial functions and brain-body-tool integration stress further that the analysis of the cognitive system should go beyond the neural boundaries of the brain.

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The orbits and eyes of modern humans are situated directly below the frontal lobes and anterior to the temporal lobes. Contiguity between these orbital and cerebral elements could generate spatial constraints, and potentially lead to deformation of the eye and reduced visual acuity during development. In this shape analysis we evaluate whether and to what extent covariation exists between ocular morphology and the size and spatial position of the frontal and temporal areas in adult modern humans. Magnetic resonance imaging (MRI) was used to investigate patterns of variation among the brain and eyes, while computed tomography (CT) was used to compare cranial morphology in this anatomical region among modern humans, extinct hominids and chimpanzees. Seventeen landmarks and semi-landmarks that capture the outline of the eye, frontal lobe, anterior fossa/orbital roof and the position of the temporal tips were sampled using lateral scout views in two dimensions, after projection of the average grayscale values of each hemisphere, with midsagittal and parasagittal elements overlapped onto the same plane. MRI results demonstrated that eye position in adult humans varies most with regard to its horizontal distance from the temporal lobes and, secondly, in its vertical distance from the frontal lobes. Size was mainly found to covary with the distance between the eye and temporal lobes. Proximity to these cerebral lobes may generate spatial constraints, as some ocular deformation was observed. Considering the CT analysis, modern humans vary most with regard to the orientation of the orbits, while interspecific variation is mainly associated with separation between the orbits and endocranial elements. These findings suggest that size and position of the frontal and temporal lobes can affect eye and orbit morphology, though potential effects on eye shape require further study. In particular, possible effects of these spatial and allometric relationships on the eye and vision should be examined using ontogenetic samples, vision parameters such as refractive error in diopters, and three-dimensional approaches that include measures of extraocular soft tissues within the orbit.

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Modern humans have evolved bulging parietal areas and large, projecting temporal lobes. Both changes, largely due to a longitudinal expansion of these cranial and cerebral elements, were hypothesized to be the result of brain evolution and cognitive variations. Nonetheless, the independence of these two morphological characters has not been evaluated. Because of structural and functional integration among cranial elements, changes in the position of the temporal poles can be a secondary consequence of parietal bulging and reorientation of the head axis. In this study, we use geometric morphometrics to test the correlation between parietal shape and the morphology of the endocranial base in a sample of adult modern humans. Our results suggest that parietal proportions show no correlation with the relative position of the temporal poles within the spatial organization of the endocranial base. The vault and endocranial base are likely to be involved in distinct morphogenetic processes, with scarce or no integration between these two districts. Therefore, the current evidence rejects the hypothesis of reciprocal morphological influences between parietal and temporal morphology, suggesting that evolutionary spatial changes in these two areas may have been independent. However, parietal bulging exerts a visible effect on the rotation of the cranial base, influencing head position and orientation. This change can have had a major relevance in the reorganization of the head functional axis.

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